Effector loss drives adaptation of Pseudomonas syringae pv. actinidiae biovar 3 to Actinidia arguta

• DOI: 10.1371/journal.ppat.1010542
• Publication Date: 2022-05-27T17:41:16Z
• Authors: Lauren M. Hemara; Jay Jayaraman; Paul W. Sutherland; Mirco Montefiori; Saadiah Arshed; Abhishek Chatterjee; Ronan Chen; Mark T. Andersen; Carl H. Mesarich; Otto van der Linden; Minsoo Yoon; Magan M. Schipper; Joel L. Vanneste; Cyril Brendolise; Matthew D. Templeton
• Keywords: Plant Leaves; 0301 basic medicine; 0303 health sciences; 03 medical and health sciences; Virulence; QH301-705.5; Actinidia; Pseudomonas syringae; Immunologic diseases. Allergy; RC581-607; Biology (General); Research Article; Plant Diseases

A pandemic isolate ofPseudomonas syringaepv.actinidiaebiovar 3 (Psa3) has devastated kiwifruit orchards growing cultivars ofActinidia chinensis. In contrast,A.arguta(kiwiberry) is not a host of Psa3. Resistance is mediated via effector-triggered immunity, as demonstrated by induction of the hypersensitive response in infectedA.argutaleaves, observed by microscopy and quantified by ion-leakage assays. Isolates of Psa3 that cause disease inA.argutahave been isolated and analyzed, revealing a 51 kb deletion in the exchangeable effector locus (EEL). This natural EEL-mutant isolate and strains with synthetic knockouts of the EEL were more virulent inA.argutaplantlets than wild-type Psa3. Screening of a complete library of Psa3 effector knockout strains identified increased growthin plantafor knockouts of four effectors–AvrRpm1a, HopF1c, HopZ5a, and the EEL effector HopAW1a –suggesting a resistance response inA.arguta. Hypersensitive response (HR) assays indicate that three of these effectors trigger a host species-specific HR. A Psa3 strain with all four effectors knocked out escaped host recognition, but a cumulative increase in bacterial pathogenicity and virulence was not observed. These avirulence effectors can be used in turn to identify the first cognate resistance genes inActinidiafor breeding durable resistance into future kiwifruit cultivars.